Abstract for CNS 2016 in New York, NY: Constructing a rich egocentric representation of one’s movement about an environment is a multi-faceted effort requiring a vast interplay across cortical areas responsible for visual processing, heading direction, and spatial coding. While electrophysiological recordings in rodents have identified robust neural correlates related to distinct aspects of navigation, experimental work with human subjects offers the unique potential to elucidate the mechanisms of navigational mental imagery, a process we frequently engage in when planning a route or giving directions. In the present study, we first familiarized participants with navigational paths about three highly distinctive virtual environments. The next day, while undergoing fMRI scanning, participants viewed a series of first-person videos that indicated either clockwise or counter-clockwise movement around the perimeter of each environment. After several rounds of video viewing, participants performed a new task in which they were covertly cued to imagine themselves walking along each of these same routes. We leveraged support vector machines within a searchlight-mapping approach to identify brain regions whose BOLD patterns coded for information pertaining to the participants’ heading direction or environmental context. As anticipated, many visual association regions with significant accuracy for decoding the contents of perceived navigation were also capable of decoding imagined navigation, although imagery classification performance was generally less robust. Interestingly, several frontal and temporal lobe regions showed decoding effects that were specific to mental imagery, and the distribution of these areas differed as a function of gender, potentially indicative of a qualitatively different mental representation of navigational information across males and females.